High incidence of adverse cerebral blood flow responses to spreading depolarization in the aged ischemic rat brain

Neurobiology of Aging

Volumn 36, Issue 12, 2015, Pages 3269-3277

  Menyhárt, Ákos ^a   Makra, Péter ^a   Szepes, Borbála E ^a   Tóth, Orsolya M ^a   Hertelendy, Péter ^a   Bari, Ferenc ^a   Farkas, Eszter ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Aging; Cerebral blood flow; Cerebral ischemia; Electrophysiology; Rat; Spreading depolarization

Indexed keywords

POTASSIUM CHLORIDE;

ADULT; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN BLOOD FLOW; BRAIN ISCHEMIA; BRAIN SPREADING DEPOLARIZATION; CAROTID ARTERY OBSTRUCTION; COMMON CAROTID ARTERY; CONTROLLED STUDY; CORTICAL DIRECT CURRENT POTENTIAL; CRANIOTOMY; ELECTROCORTICOGRAPHY; INCIDENCE; MALE; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PARIETAL CORTEX; PRIORITY JOURNAL; RAT; SHAM PROCEDURE; ANIMAL; BRAIN; BRAIN CIRCULATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VASCULARIZATION; WISTAR RAT;

AGING; ANIMALS; BRAIN; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; ELECTROCORTICOGRAPHY; MALE; RATS, SPRAGUE-DAWLEY; RATS, WISTAR;

EID: 84947030025     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.08.014     Document Type: Article

References (47)

1. Astrup J., Symon L., Branston N.M., Lassen N.A. Cortical evoked potential and extracellular K+ and H+ at critical levels of brain ischemia. Stroke 1977, 8:51-57.
2. Ay H., Koroshetz W.J., Vangel M., Benner T., Melinosky C., Zhu M., Menezes N., Lopez C.J., Sorensen A.G. Conversion of ischemic brain tissue into infarction increases with age. Stroke 2005, 36:2632-2636.
3. Ayata C. Spreading depression and neurovascular coupling. Stroke 2013, 44(6 Suppl 1):S87-S89.
4. Back T., Ginsberg M.D., Dietrich W.D., Watson B.D. Induction of spreading depression in the ischemic hemisphere following experimental middle cerebral artery occlusion: effect on infarct morphology. J. Cereb. Blood Flow Metab. 1996, 16:202-213.
5. Bere Z., Obrenovitch T.P., Bari F., Farkas E. Ischemia-induced depolarizations and associated hemodynamic responses in incomplete global forebrain ischemia in rats. Neuroscience 2014, 260:217-226.
6. Bere Z., Obrenovitch T.P., Kozák G., Bari F., Farkas E. Imaging reveals the focal area of spreading depolarizations and a variety of hemodynamic responses in a rat microembolic stroke model. J. Cereb. Blood Flow Metab. 2014, 34:1695-1705.
7. Chen R.L., Balami J.S., Esiri M.M., Chen L.K., Buchan A.M. Ischemic stroke in the elderly: an overview of evidence. Nat. Rev. Neurol. 2010, 6:256-265.
8. Claassen J., Hirsch L.J., Kreiter K.T., Du E.Y., Connolly E.S., Emerson R.G., Mayer S.A. Quantitative continuous EEG for detecting delayed cerebral ischemia in patients with poor-grade subarachnoid hemorrh age. Clin. Neurophysiol 2004, 115:2699-2710.
9. Clark D., Institoris A., Kozák G., Bere Z., Tuor U., Farkas E., Bari F. Impact of aging on spreading depolarizations induced by focal brain ischemia in rats. Neurobiol. Aging 2014, 35:2803-2811.
10. Dohmen C., Sakowitz O.W., Fabricius M., Bosche B., Reithmeier T., Ernestus R.I., Brinker G., Dreier J.P., Woitzik J., Strong A.J., Graf R. Spreading depolarizations occur in human ischemic stroke with high incidence. Ann. Neurol. 2008, 63:720-728. Co-Operative Study of Brain Injury Depolarisations (COSBID).
11. Dougherty P.M., Li Y.J., Lenz F.A., Rowland L., Mittman S. Correlation of effects of general anesthetics on somatosensory neurons in the primate thalamus and cortical EEG power. J. Neurophysiol. 1997, 77:1375-1392.
12. Dreier J.P. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat. Med. 2011, 17:439-447.
13. Dreier J.P., Körner K., Ebert N., Görner A., Rubin I., Back T., Lindauer U., Wolf T., Villringer A., Einhäupl K.M., Lauritzen M., Dirnagl U. Nitric oxide scavenging by hemoglobin or nitric oxide synthase inhibition by N-nitro-L-arginine induces cortical spreading ischemia when K+ is increased in the subarachnoid space. J. Cereb. Blood Flow Metab. 1998, 18:978-990.
14. Dreier J.P., Petzold G., Tille K., Lindauer U., Arnold G., Heinemann U., Einhäupl K.M., Dirnagl U. Ischaemia triggered by spreading neuronal activation is inhibited by vasodilators in rats. J. Physiol. 2001, 531(Pt 2):515-526.
15. Dreier J.P., Woitzik J., Fabricius M., Bhatia R., Major S., Drenckhahn C., Lehmann T.N., Sarrafzadeh A., Willumsen L., Hartings J.A., Sakowitz O.W., Seemann J.H., Thieme A., Lauritzen M., Strong A.J. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 2006, 129(Pt 12):3224-3237.
16. Dugan L.L., Choi D.W. Hypoxia-ischemia and brain infarction. Basic Neurochemistry: Molecular, Cellular and Medical Aspects 1999, 711-730. Lippincott-Raven, Philadelphia. G.J. Siegel, B.W. Agranoff, R.W. Albers, S.K. Fisher, M.D. Uhler (Eds.).
17. Duverger D., MacKenzie E.T. The quantification of cerebral infarction following focal ischemia in the rat: influence of strain, arterial pressure, blood glucose concentration, and age. J. Cereb. Blood Flow Metab. 1988, 8:449-461.
18. Faber J.E., Zhang H., Lassance-Soares R.M., Prabhakar P., Najafi A.H., Burnett M.S., Epstein S.E. Aging causes collateral rarefaction and increased severity of ischemic injury in multiple tissues. Arterioscler. Thromb. Vasc. Biol. 2011, 31:1748-1756.
19. Farkas E., Bari F. Spreading depolarization in the ischemic brain: does aging have an impact?. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69:1363-1370.
20. Farkas E., Luiten P.G. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog. Neurobiol. 2001, 64:575-611.
21. Farkas E., Obrenovitch T.P., Institóris Á., Bari F. Effects of early aging and cerebral hypoperfusion on spreading depression in rats. Neurobiol. Aging 2011, 32:1707-1715.
22. Fox G., Gallacher D., Shevde S., Loftus J., Swayne G. Anatomic variation of the middle cerebral artery in the Sprague-Dawley rat. Stroke 1993, 24:2087-2092. discussion 2092-3.
23. Hansen A.J., Quistorff B., Gjedde A. Relationship between local changes in cortical blood flow and extracellular K+ during spreading depression. Acta Physiol. Scand. 1980, 109(1):1-6.
24. Hansen A.J., Zeuthen T. Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. Acta Physiol. Scand. 1981, 113:437-445.
25. Hartings J.A., Watanabe T., Bullock M.R., Okonkwo D.O., Fabricius M., Woitzik J., Dreier J.P., Puccio A., Shutter L.A., Pahl C., Strong A.J. Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. Brain 2011, 134(Pt 5):1529-1540. Co-Operative Study on Brain Injury Depolarizations.
26. Hartings J.A., Watanabe T., Dreier J.P., Major S., Vendelbo L., Fabricius M. Recovery of slow potentials in AC-coupled electrocorticography: application to spreading depolarizations in rat and human cerebral cortex. J. Neurophysiol. 2009, 102:2563-2575.
27. Hoffmann U., Ayata C. Neurovascular coupling during spreading depolarizations. Acta Neurochir Suppl. 2013, 115:161-165.
28. Lapi D., Colantuoni A. Remodeling of cerebral microcirculation after ischemia-reperfusion. J. Vasc. Res. 2015, 52:22-31.
29. Leão A.A.P. Spreading depression of activity in the cerebral cortex. J. Neurophysiol. 1944, 7:359-390.
30. Liao L.D., Liu Y.H., Lai H.Y., Bandla A., Shih Y.Y., Chen Y.Y., Thakor N.V. Rescue of cortical neurovascular functions during the hyperacute phase of ischemia by peripheral sensory stimulation. Neurobiol. Dis. 2015, 75:53-63.
31. Liu F., McCullough L.D. Interactions between age, sex, and hormones in experimental ischemic stroke. Neurochem. Int. 2012, 61:1255-1265.
32. Liu F., Yuan R., Benashski S.E., McCullough L.D. Changes in experimental stroke outcome across the life span. J. Cereb. Blood Flow Metab. 2009, 29:792-802.
33. Maslarova A., Alam M., Reiffurth C., Lapilover E., Gorji A., Dreier J.P. Chronically epileptic human and rat neocortex display a similar resistance against spreading depolarization in vitro. Stroke 2011, 42:2917-2922.
34. Mayhan W.G., Arrick D.M., Sharpe G.M., Sun H. Age-related alterations in reactivity of cerebral arterioles: role of oxidative stress. Microcirculation 2008, 15:225-236.
35. Nedergaard M. Spreading depression as a contributor to ischemic brain damage. Adv. Neurol. 1996, 71:75-83. discussion 83-4.
36. Park L., Anrather J., Girouard H., Zhou P., Iadecola C. Nox2-derived reactive oxygen species mediate neurovascular dysregulation in the aging mouse brain. J. Cereb. Blood Flow Metab. 2007, 27:1908-1918.
37. Popa-Wagner A., Badan I., Walker L., Groppa S., Patrana N., Kessler C. Accelerated infarct development, cytogenesis and apoptosis following transient cerebral ischemia in aged rats. Acta Neuropathol. 2007, 113:277-293.
38. Rossi D.J., Brady J.D., Mohr C. Astrocyte metabolism and signaling during brain ischemia. Nat. Neurosci. 2007, 10:1377-1386.
39. Rubino G.J., Young W. Ischemic cortical lesions after permanent occlusion of individual middle cerebral artery branches in rats. Stroke 1988, 19:870-877.
40. Obrenovitch T.P., Chen S., Farkas E. Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods. Neuroimage 2009, 45:68-74.
41. Shin H.K., Dunn A.K., Jones P.B., Boas D.A., Moskowitz M.A., Ayata C. Vasoconstrictive neurovascular coupling during focal ischemic depolarizations. J. Cereb. Blood Flow Metab. 2006, 26:1018-1030.
42. Somjen G.G. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 2001, 81:1065-1096.
43. Strong A.J., Fabricius M., Boutelle M.G., Hibbins S.J., Hopwood S.E., Jones R., Parkin M.C., Lauritzen M. Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke 2002, 33:2738-2743.
44. Ungvari Z., Kaley G., de Cabo R., Sonntag W.E., Csiszar A. Mechanisms of vascular aging: new perspectives. J. Gerontol. A Biol. Sci. Med. Sci. 2010, 65:1028-1041.
45. Warner D.S., Sheng H., Batinić-Haberle I. Oxidants, antioxidants and the ischemic brain. J. Exp. Biol. 2004, 207(Pt 18):3221-3231.
46. Windmüller O., Lindauer U., Foddis M., Einhäupl K.M., Dirnagl U., Heinemann U., Dreier J.P. Ion changes in spreading ischaemia induce rat middle cerebral artery constriction in the absence of NO. Brain 2005, 128:2042-2051.
47. Woitzik J., Hecht N., Pinczolits A., Sandow N., Major S., Winkler M.K., Weber-Carstens S., Dohmen C., Graf R., Strong A.J., Dreier J.P., Vajkoczy P. Propagation of cortical spreading depolarization in the human cortex after malignant stroke. Neurology 2013, 80:1095-1102. COSBID study group.